Genomic and Phenotypic Analyses Reveal the Emergence of an Atypical Salmonella enterica Serovar Senftenberg Variant in China

Handle URI:
http://hdl.handle.net/10754/618379
Title:
Genomic and Phenotypic Analyses Reveal the Emergence of an Atypical Salmonella enterica Serovar Senftenberg Variant in China
Authors:
Abd El Ghany, Moataz; Shi, Xiaolu; Li, Yinghui; Ansari, Hifzur Rahman ( 0000-0002-0646-1743 ) ; Hill-Cawthorne, Grant A.; Ho, Y. S.; Naeem, Raeece ( 0000-0003-1734-1007 ) ; Pickard, Derek; Klena, John D.; Xu, Xuebing; Pain, Arnab ( 0000-0002-1755-2819 ) ; Hu, Qinghua
Abstract:
Human infections with Salmonella enterica subspecies enterica serovar Senftenberg are often associated with exposure to poultry flocks, farm environments, or contaminated food. The recent emergence of multidrug-resistant isolates has raised public health concerns. In this study, comparative genomics and phenotypic analysis were used to characterize 14 Salmonella Senftenberg clinical isolates recovered from multiple outbreaks in Shenzhen and Shanghai, China, between 2002 and 2011. Single-nucleotide polymorphism analyses identified two phylogenetically distinct clades of S. Senftenberg, designated SC1 and SC2, harboring variations in Salmonella pathogenicity island 1 (SPI-1) and SPI-2 and exhibiting distinct biochemical and phenotypic signatures. Although the two variants shared the same serotype, the SC2 isolates of sequence type 14 (ST14) harbored intact SPI-1 and -2 and hence were characterized by possessing efficient invasion capabilities. In contrast, the SC1 isolates had structural deletion patterns in both SPI-1 and -2 that correlated with an impaired capacity to invade cultured human cells and also the year of their isolation. These atypical SC1 isolates also lacked the capacity to produce hydrogen sulfide. These findings highlight the emergence of atypical Salmonella Senftenberg variants in China and provide genetic validation that variants lacking SPI-1 and regions of SPI-2, which leads to impaired invasion capacity, can still cause clinical disease. These data have identified an emerging public health concern and highlight the need to strengthen surveillance to detect the prevalence and transmission of nontyphoidal Salmonella species.
KAUST Department:
Biological and Environmental Sciences & Engineering Division (BESE)
Citation:
Genomic and Phenotypic Analyses Reveal the Emergence of an Atypical Salmonella enterica Serovar Senftenberg Variant in China 2016, 54 (8):2014 Journal of Clinical Microbiology
Journal:
Journal of Clinical Microbiology
Issue Date:
25-May-2016
DOI:
10.1128/JCM.00052-16
Type:
Article
ISSN:
0095-1137; 1098-660X
Sponsors:
This work, including the efforts of Qinghua Hu, was funded by The National Science Foundation of China (81071433). This work, including the efforts of Qinghua Hu, was funded by China National Science and Technology Major Project Foundation (2012ZX10004215-003-005 and 2016ZX10004215-005-005). This work, including the efforts of Qinghua Hu, was funded by Shenzhen Public Service Platform of Pathogenic Microorganisms Repository. This work, including the efforts of Arnab Pain, was funded by Faculty Baseline Research Funds (KAUST-BRF).
Additional Links:
http://jcm.asm.org/lookup/doi/10.1128/JCM.00052-16
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Articles

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DC FieldValue Language
dc.contributor.authorAbd El Ghany, Moatazen
dc.contributor.authorShi, Xiaoluen
dc.contributor.authorLi, Yinghuien
dc.contributor.authorAnsari, Hifzur Rahmanen
dc.contributor.authorHill-Cawthorne, Grant A.en
dc.contributor.authorHo, Y. S.en
dc.contributor.authorNaeem, Raeeceen
dc.contributor.authorPickard, Dereken
dc.contributor.authorKlena, John D.en
dc.contributor.authorXu, Xuebingen
dc.contributor.authorPain, Arnaben
dc.contributor.authorHu, Qinghuaen
dc.date.accessioned2016-08-14T09:30:45Z-
dc.date.available2016-08-14T09:30:45Z-
dc.date.issued2016-05-25-
dc.identifier.citationGenomic and Phenotypic Analyses Reveal the Emergence of an Atypical Salmonella enterica Serovar Senftenberg Variant in China 2016, 54 (8):2014 Journal of Clinical Microbiologyen
dc.identifier.issn0095-1137-
dc.identifier.issn1098-660X-
dc.identifier.doi10.1128/JCM.00052-16-
dc.identifier.urihttp://hdl.handle.net/10754/618379-
dc.description.abstractHuman infections with Salmonella enterica subspecies enterica serovar Senftenberg are often associated with exposure to poultry flocks, farm environments, or contaminated food. The recent emergence of multidrug-resistant isolates has raised public health concerns. In this study, comparative genomics and phenotypic analysis were used to characterize 14 Salmonella Senftenberg clinical isolates recovered from multiple outbreaks in Shenzhen and Shanghai, China, between 2002 and 2011. Single-nucleotide polymorphism analyses identified two phylogenetically distinct clades of S. Senftenberg, designated SC1 and SC2, harboring variations in Salmonella pathogenicity island 1 (SPI-1) and SPI-2 and exhibiting distinct biochemical and phenotypic signatures. Although the two variants shared the same serotype, the SC2 isolates of sequence type 14 (ST14) harbored intact SPI-1 and -2 and hence were characterized by possessing efficient invasion capabilities. In contrast, the SC1 isolates had structural deletion patterns in both SPI-1 and -2 that correlated with an impaired capacity to invade cultured human cells and also the year of their isolation. These atypical SC1 isolates also lacked the capacity to produce hydrogen sulfide. These findings highlight the emergence of atypical Salmonella Senftenberg variants in China and provide genetic validation that variants lacking SPI-1 and regions of SPI-2, which leads to impaired invasion capacity, can still cause clinical disease. These data have identified an emerging public health concern and highlight the need to strengthen surveillance to detect the prevalence and transmission of nontyphoidal Salmonella species.en
dc.description.sponsorshipThis work, including the efforts of Qinghua Hu, was funded by The National Science Foundation of China (81071433). This work, including the efforts of Qinghua Hu, was funded by China National Science and Technology Major Project Foundation (2012ZX10004215-003-005 and 2016ZX10004215-005-005). This work, including the efforts of Qinghua Hu, was funded by Shenzhen Public Service Platform of Pathogenic Microorganisms Repository. This work, including the efforts of Arnab Pain, was funded by Faculty Baseline Research Funds (KAUST-BRF).en
dc.language.isoenen
dc.relation.urlhttp://jcm.asm.org/lookup/doi/10.1128/JCM.00052-16en
dc.rightsArchived with thanks to Journal of Clinical Microbiologyen
dc.titleGenomic and Phenotypic Analyses Reveal the Emergence of an Atypical Salmonella enterica Serovar Senftenberg Variant in Chinaen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences & Engineering Division (BESE)en
dc.identifier.journalJournal of Clinical Microbiologyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionShenzhen Centre for Disease Control and Prevention, Shenzhen, Guangdong Province, Chinaen
dc.contributor.institutionMarie Bashir Institute for Infectious Diseases and Biosecurity and School of Public Health, University of Sydney, Sydney, Australiaen
dc.contributor.institutionThe Wellcome Trust Sanger Institute (WTSI), the Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdomen
dc.contributor.institutionCenters for Disease Control and Prevention, Atlanta, Georgia, USAen
dc.contributor.institutionShanghai Municipal Center for Disease Control and Prevention, Shanghai, Chinaen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorEl Ghany, Moataz Abden
kaust.authorAnsari, Hifzur Rahmanen
kaust.authorHo, Y. S.en
kaust.authorNaeem, Raeeceen
kaust.authorPain, Arnaben
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